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Population clustering of structural brain aging and its association with brain development.

Authors
  • Duan, Haojing1, 2
  • Shi, Runye3
  • Kang, Jujiao1, 2
  • Banaschewski, Tobias4
  • Bokde, Arun L W5
  • Büchel, Christian6
  • Desrivières, Sylvane7
  • Flor, Herta8, 9
  • Grigis, Antoine10
  • Garavan, Hugh11
  • Gowland, Penny A12
  • Heinz, Andreas13
  • Brühl, Rüdiger14
  • Martinot, Jean-Luc15
  • Martinot, Marie-Laure Paillère15, 16
  • Artiges, Eric15, 17
  • Nees, Frauke4, 8, 18
  • Papadopoulos Orfanos, Dimitri10
  • Poustka, Luise19
  • Hohmann, Sarah4
  • And 9 more
  • 1 Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China. , (China)
  • 2 Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence (Fudan University), Ministry of Education, Shanghai, China. , (China)
  • 3 School of Data Science, Fudan University, Shanghai, China. , (China)
  • 4 Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany. , (Germany)
  • 5 Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin, Ireland. , (Ireland)
  • 6 University Medical Centre Hamburg-Eppendorf, Hamburg, Germany. , (Germany)
  • 7 Social Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom. , (United Kingdom)
  • 8 Institute of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany. , (Germany)
  • 9 Department of Psychology, School of Social Sciences, University of Mannheim, Mannheim, Germany. , (Germany)
  • 10 NeuroSpin, CEA, Université Paris-Saclay, Gif-sur-Yvette, France. , (France)
  • 11 Departments of Psychiatry and Psychology, University of Vermont, Burlington, United States. , (United States)
  • 12 Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, Nottingham, United Kingdom. , (United Kingdom)
  • 13 Department of Psychiatry and Psychotherapy CCM, Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany. , (Germany)
  • 14 Physikalisch-Technische Bundesanstalt (PTB), Braunschweig and Berlin, Berlin, Germany. , (Germany)
  • 15 Institut National de la Santé et de la Recherche Médicale, INSERM U1299 "Developmental Trajectories and Psychiatry", Université Paris-Saclay, Ecole Normale supérieure Paris-Saclay, CNRS, Centre Borelli, Gif-sur-Yvette, France. , (France)
  • 16 AP-HP. Sorbonne Université, Department of Child and Adolescent Psychiatry, Pitié-Salpêtrière Hospital, Paris, France. , (France)
  • 17 Psychiatry Department, EPS Barthélémy Durand, Etampes, France. , (France)
  • 18 Institute of Medical Psychology and Medical Sociology, University Medical Center Schleswig-Holstein, Kiel University, Kiel, Germany. , (Germany)
  • 19 Department of Child and Adolescent Psychiatry and Psychotherapy, University Medical Centre, Göttingen, Germany. , (Germany)
  • 20 Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany. , (Germany)
  • 21 Department of Psychiatry and Neurosciences, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität BerlinHumboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany. , (Germany)
  • 22 School of Psychology and Global Brain Health Institute, Trinity College Dublin, Dublin, Ireland. , (Ireland)
  • 23 Centre for Population Neuroscience and Stratified Medicine (PONS Centre), ISTBI, Fudan University, Shanghai, China. , (China)
  • 24 Centre for Population Neuroscience and Stratified Medicine (PONS), Department of Psychiatry and Psychotherapy, Charité Universitätsmedizin, Berlin, Germany. , (Germany)
  • 25 Huashan Institute of Medicine, Huashan Hospital affiliated to Fudan University, Shanghai, China. , (China)
  • 26 MOE Frontiers Center for Brain Science, Fudan University, Shanghai, China. , (China)
  • 27 Zhangjiang Fudan International Innovation Center, Shanghai, China. , (China)
  • 28 Department of Computer Science, University of Warwick, Warwick, United Kingdom. , (United Kingdom)
Type
Published Article
Journal
eLife
Publisher
"eLife Sciences Organisation, Ltd."
Publication Date
Oct 18, 2024
Volume
13
Identifiers
DOI: 10.7554/eLife.94970
PMID: 39422662
Source
Medline
Keywords
Language
English
License
Unknown

Abstract

Structural brain aging has demonstrated strong inter-individual heterogeneity and mirroring patterns with brain development. However, due to the lack of large-scale longitudinal neuroimaging studies, most of the existing research focused on the cross-sectional changes of brain aging. In this investigation, we present a data-driven approach that incorporate both cross-sectional changes and longitudinal trajectories of structural brain aging and identified two brain aging patterns among 37,013 healthy participants from UK Biobank. Participants with accelerated brain aging also demonstrated accelerated biological aging, cognitive decline and increased genetic susceptibilities to major neuropsychiatric disorders. Further, by integrating longitudinal neuroimaging studies from a multi-center adolescent cohort, we validated the 'last in, first out' mirroring hypothesis and identified brain regions with manifested mirroring patterns between brain aging and brain development. Genomic analyses revealed risk loci and genes contributing to accelerated brain aging and delayed brain development, providing molecular basis for elucidating the biological mechanisms underlying brain aging and related disorders. © 2024, Duan et al.

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